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Serial Third-Trimester Ultrasonography Compared With Routine Care in Uncomplicated Pregnancies

A Randomized Controlled Trial

Ashimi Balogun, Olaide, MD; Sibai, Baha M., MD; Pedroza, Claudia, PhD; Blackwell, Sean C., MD; Barrett, Tyisha L.; Chauhan, Suneet P., MD, HonDSc

doi: 10.1097/AOG.0000000000002970
Contents: Ultrasonography: Original Research
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OBJECTIVE: Among uncomplicated pregnancies, serial third-trimester ultrasound examinations identified significantly more cases with a composite of fetal growth or amniotic fluid abnormalities (27%) than did routine fundal height measurements (8%).

METHODS: Women without complications between 24 0/7 and 30 6/7 weeks of gestation were randomized (NCT0270299) to either routine care (control arm) or ultrasound examination every 4 weeks (intervention arm). The primary outcome was a composite of abnormalities of fluid volume and growth: oligohydramnios or polyhydramnios; fetal growth restriction; or large for gestational age. The secondary outcome was the presence of composite maternal or neonatal morbidity among the two groups. A total of 206 participants was needed to have 80% power to detect an increase in the primary composite outcome from 10% in control to 25% in the intervention group (baseline rate 10%; two-tailed; α=0.05; loss to follow-up 5%). All women were included in the intent-to-treat analysis. Fisher exact, χ2 tests, or two-sample t tests were used to assess group differences.

RESULTS: From July 11, 2016, to May 24, 2017, 852 women were screened for eligibility and 206 were randomized as follows: 102 in routine care and 104 in serial ultrasound examinations. The two groups were comparable in baseline characteristics. The primary composite outcome was significantly higher among women who were in the ultrasound examination group than the routine care group (27% vs 8%; relative risk 3.43, 95% CI 1.64–7.17); five women (95% CI 3–11) were needed to identify at least one of the composite ultrasound abnormalities. Although we were underpowered to detect a significant difference, the following secondary endpoints occurred with similar frequency in the ultrasound examination group than the routine care group: induction resulting from abnormal ultrasound examination findings (14% vs 6%), cesarean delivery in labor (5% vs 6%), and prespecified composite maternal morbidity (9% in both groups) and composite neonatal morbidity (1% vs 4%).

CONCLUSION: Among uncomplicated pregnancies between 24 0/7 and 30 6/7 weeks of gestation, serial third-trimester ultrasound examinations were significantly more likely to identify abnormalities of fetal growth or amniotic fluid than measurements of fundal height and indicated ultrasound examination. No differences in maternal and neonatal outcomes were noted, although we were underpowered for these endpoints.

CLINICAL TRIAL REGISTRATION: ClinicalTrials.gov, NCT02702999.

Department of Obstetrics, Gynecology, and Reproductive Sciences, McGovern Medical School, and the Center for Clinical Research and Evidence-Based Medicine, Department of Pediatrics, University of Texas Health Science Center at Houston, Houston, Texas.

Corresponding author: Olaide Ashimi Balogun, MD, Department of Obstetrics, Gynecology, and Reproductive Sciences, University of Texas Health Science Center at Houston, 6431 Fannin Street, MSB 3.270 Houston, TX 77030; email: Olaide.A.Ashimi@uth.tmc.edu.

Supported in part by the Larry C. Gilstrap MD Center for Perinatal and Women’s Health Research.

Financial Disclosure The authors did not report any potential conflicts of interest.

Presented at the 37th annual meeting of the Society for Maternal-Fetal Medicine, January 29–February 3, 2018, Dallas, Texas.

Each author has indicated that he or she has met the journal’s requirements for authorship.

Peer review history is available at http://links.lww.com/AOG/B189.

Currently, the American College of Obstetricians and Gynecologists (ACOG) recommends that the first step in screening for abnormalities of fetal growth or amniotic fluid volume in uncomplicated pregnancies is serial measurements of fundal height, starting at 24 weeks of gestation. If a discrepancy between gestational age and measurement of the fundus is present, the second step is to obtain an ultrasound examination to assess fetal weight and amniotic fluid volume.1,2 As a result of routine care, a substantial portion of small for gestational age (birth weight less than the 10th percentile for gestational age) or large for gestational age (LGA; birth weight greater than the 90th percentile for gestational age) and oligohydramnios or polyhydramnios is unidentified3–6 and therefore may not benefit from antepartum surveillance and interventions.7–9

Abnormal growth occurs in 16% of uncomplicated pregnancies.10 These pregnancies are more likely to result in stillbirths or have neonates with morbidities.11–13 Abnormalities of amniotic fluid volume—oligohydramnios or polyhydramnios—occur in up to 10% of low-risk pregnancies and are associated with stillbirth, low Apgar score, and neonatal mortality.6,14–17 There is an impetus to improve the identification of fetal growth restriction (estimated fetal weight less than the 10th percentile for gestational age), ultrasonographic LGA (estimated fetal weight greater than the 90th percentile for gestational age), oligohydramnios, and polyhydramnios.

The purpose of this randomized clinical trial was to compare the identification of composite of abnormalities of fluid volume and growth—oligohydramnios, polyhydramnios, fetal growth restriction, or ultrasonographic LGA—in uncomplicated pregnancies by performing serial fundal height measurements and ultrasound examination if there was a discrepancy compared with serial ultrasound examination every 4 weeks, regardless of the measurement of fundal height. We focused on this composite because after a normal second-trimester anatomy ultrasound examination, these are the most common abnormalities identified6 and because the purpose of fundal height measurements is to screen for these four abnormal conditions.

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MATERIALS AND METHODS

This single-centered randomized controlled trial commenced after obtaining approval from institutional review board at The McGovern Medical School–University of Texas at Houston and registering on ClinicalTrials.gov (NCT0270299). Inclusion criteria were women who were at least 18 years old, had a singleton pregnancy with no major prenatally diagnosed fetal anomalies, and who had an estimated due date based on in vitro fertilization or ultrasound examination before 22 0/7 weeks.18 Women were excluded for any medical complication or comorbidity at the time of randomization (Box 1). If a complication developed after randomization, women remained in the group to which they were randomized.

Trained research staff approached eligible women and obtained informed, written consent between 24 0/7 to 30 6/7 weeks of gestation after it was determined they did not have gestational diabetes.19 Enrolled participants were randomly assigned in a one-to-one ratio using permuted block randomization to prevent imbalances between groups. The random allocation sequence was developed in R software by the statistician (C.P.) who was not involved in the conduct of the study. The randomization table was uploaded to REDCap. Treatment allocation was assigned through the randomization module. Participants were assigned to either routine care, which included serial fundal height measurements at each clinical appointment prompting an ultrasound examination if a discrepancy was present (routine arm), or ultrasound examination every 4 weeks (at approximately 30, 34, and 38 weeks of gestation), regardless of fundal height measurements (intervention arm). Women enrolled, ultrasonographers, and maternal–fetal medicine attendings reviewing the ultrasound examinations and the chart abstractor were not blinded to the group allocation.

Clinicians treating these women were informed of the ultrasound findings if any of the following were noted: fetal growth restriction, LGA, oligohydramnios, polyhydramnios, or any ultrasound findings that would influence clinical treatment (eg, spontaneous bradycardia or previously undetected fetal anomaly). Women with abnormal findings were notified. The clinicians treated their patients according to ACOG guidelines.1,7,8 In both groups, additional ultrasound examinations could be obtained if deemed necessary by the obstetric care provider if complications developed (eg, preterm labor, decreased fetal movements, or development of hypertensive disease). Registered diagnostic medical ultrasonographers did all the ultrasound examinations and a maternal–fetal medicine subspecialist reviewed all ultrasound examinations. Obstetrics–gynecology faculty and residents training under their supervision did all of the fundal height measurements. To reflect daily clinical practice, standardization of measurements of biometric parts, amniotic fluid, or fundal height was not done for this trial.

The fetal weight was estimated by obtaining measurements of the biparietal diameter, head circumference, abdominal circumference, and femoral diaphysis length. The regression equation proposed by Hadlock et al20 was used to estimate the fetal weight. Fetal growth abnormalities were defined if the estimated fetal weight was less than the 10th percentile or greater than the 90th percentile for gestational age.1,21,22 Amniotic fluid was assessed using either the amniotic fluid index or maximum vertical pocket. Oligohydramnios was defined as amniotic fluid index 5.0 cm or less or maximum vertical pocket 2.0 cm or less. Polyhydramnios was defined as an amniotic fluid index 24.0 or greater or maximum vertical pocket 8.0 cm or greater.2 All ultrasound reports were made available to the treating health care providers. Decision-making regarding the management of each pregnancy was at the discretion of the individual clinician. The nomogram published by Alexander et al23 was used to categorize newborns as small for gestational age (birth weight less than the 10th percentile for gestational age) or as actual LGA (birth weight greater than the 90th percentile for gestational age).

Women recruited to the study were followed through delivery and information about the remainder of their antepartum care; intrapartum and neonatal outcomes were abstracted. To keep abstracted data consistent, one author (O.A.B.) reviewed all the charts and was aware of the group allocation. Composite maternal morbidity for this trial was defined as any of the following: 1) chorioamnionitis, 2) cesarean delivery in labor, 3) wound infection, 4) transfusion, 5) deep venous thrombus or pulmonary embolism, 6) admission to the intensive care unit, or 7) death. Composite neonatal morbidity was defined as any of the following: 1) Apgar score less than 5 at 5 minutes, 2) umbilical arterial pH less than 7.00, 3) intraventricular hemorrhage grade III or IV, 4) periventricular leukomalacia, 5) intubation for longer than 24 hours, 6) necrotizing enterocolitis grade 2 or 3, 7) stillbirth after randomization, or 8) neonatal death (within 28 days) of birth in the index pregnancy.

With routine care, among uncomplicated pregnancies, the identification of the composite of abnormalities of fluid volume and growth abnormalities is 10%.6 To increase the detection of the composite of abnormalities of fluid volume and growth abnormalities from 10% in the control arm to 25% in the intervention arm, a total of 194 women needed to be randomized (α=5%; power=80%). We estimated that 5% of women would be lost to follow-up based on a previous pilot study.6 Thus, the total sample size for the trial was 206 women.

Descriptive statistics were used to summarize all study variables. Categorical variables were reported as frequencies and percentages. Fisher exact, χ2 tests, or two-sample t tests were used to assess group differences (routine vs serial ultrasound examinations) in patient outcomes. Subgroup analysis was performed using similar methods. Relative risk (RR) and 95% CI were calculated as was number needed to identify the primary composite outcome. All analyses were conducted using Stata 13.0. All randomized women were included in the intent-to-treat analysis.

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RESULTS

Recruitment began July 11, 2016, and concluded May 24, 2017. Of the 852 women screened for eligibility, 626 patients did not meet inclusion criteria. The most common reason for exclusion was women with comorbidities such as pregestational or gestational diabetes or chronic hypertension. Two hundred twenty-six women were approached to participate in the study and 20 declined. The remaining 206 women were consented and 102 were randomized to receive routine care and 104 to receive serial ultrasound examinations (Fig. 1). One woman in the routine care group delivered at an outside hospital and the outcomes of delivery were unavailable for analysis.

Figure 1.

Figure 1.

The two groups were comparable in baseline characteristics (Table 1). Women recruited in the trial were ethnically diverse, approximately 4 in 10 were nulliparous, and approximately 70% had body mass indexes (calculated as weight (kg)/[height (m)]2) less than 30 at the first prenatal visit. The total number of ultrasound examinations was higher in the intervention arm than the control arm. The indications for the ultrasound examinations differed as did the gestational age at delivery (P<.01; Table 2). The total number of antepartum complications after randomization was similar in the two groups with approximately one in four low-risk women developing a complication in their third trimester of pregnancy. The most common antepartum complication was gestational hypertension or preeclampsia (Table 3).

Table 1.

Table 1.

Table 2.

Table 2.

Table 3.

Table 3.

The primary composite outcome was more frequently identified among women who had serial ultrasound examinations than those who received routine care (27% vs 8%; RR 3.4, 95% CI 1.6–7.2). The number needed to treat was five women (95% CI 3–11). Although the study was not powered to detect differences in the individual components of the composite outcome, there was a difference in identification of polyhydramnios between the serial ultrasound examination and routine care groups (11% vs 2%; RR 5.4, 95% CI 1.2–23.7). No significant difference in the detection of fetal growth restriction, LGA, or oligohydramnios was noted (Table 4).

Table 4.

Table 4.

Analysis limited to women who did not develop any complications after randomization (eg, preterm labor or hypertensive disease) also indicated the primary composite outcome was significantly more frequent among women who had serial ultrasound examinations than routine care (27% vs 8%; RR 3.7, 95% CI 1.5–9.4). The detection of polyhydramnios differed between the two groups but the 95% CI was wide as a result of the sample size (Table 5). The number needed to treat was also five women (95% CI 3–13).

Table 5.

Table 5.

Prespecified composite maternal morbidity was similar in both groups (9% in both serial ultrasound examinations compared with routine care group; RR 1.0, 95% CI 0.4–2.3), but we were not powered to detect a difference. There were no episodes of deep venous thrombus or pulmonary embolism, admission to the intensive care unit, or maternal deaths in either groups. The prespecified composite neonatal morbidity was also similar in both groups (1% in the serial ultrasound examination group vs 4% in the routine care group; RR 0.2, 95% CI 0.03–2.1), but we were underpowered to detect a difference (Table 6).

Table 6.

Table 6.

The gestational age epoch (less than 32 0/7, 32 0/7–34 6/7, 35 0/7–36 6/7, or at least 37 0/7 weeks of gestation) when the abnormal condition was initially identified differed between the groups (P=.02). The rate of having a biophysical profile or umbilical artery Doppler, because of the abnormality noted on ultrasound examination (ie, polyhydramnios or intrauterine growth restriction), was similar between the two groups (Table 7).

Table 7.

Table 7.

Gestational age at delivery was comparable in the two groups with only 9% of women delivering before 37 weeks of gestation in both groups. The most common reason for induction of labor before 37 weeks of gestation was preeclampsia with severe features. There was no difference in delivery route between the two groups (RR 0.8, 95% CI 0.5–1.2). The most common reason for cesarean delivery in both groups was for women who declined a trial of labor and desired a repeat cesarean delivery (Table 8).

Table 8.

Table 8.

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DISCUSSION

Our randomized trial suggests that among women with uncomplicated pregnancies at 24 0/7 to 30 6/7 weeks of gestation, serial third-trimester ultrasound examinations are more likely to identify a composite of abnormalities of fetal growth or amniotic fluid than routine care. The number of women who need serial ultrasound examinations in the third trimester to identify an abnormal condition is five (95% CI 3–11). Although the trial is underpowered for assessment of peripartum outcomes, the maternal and neonatal adverse outcomes were similar as were gestational age at delivery, the rate of induction, and of cesarean delivery.

Estimates indicate that upward of two thirds of pregnancies are low risk.6,24,25 Although there are multiple potential etiologies of adverse outcomes in low-risk pregnancies, the most common ones that are amenable to interventions are aberrations of fetal growth or of amniotic fluid.6,10–17 Small-for-gestational-age and LGA newborns are significantly more likely to be stillborn and have neonatal morbidities.1,11,21 Furthermore, pregnancies complicated with oligohydramnios or polyhydramnios are associated with stillbirth, low Apgar score, and neonatal mortality.14–17 Therefore, even among uncomplicated pregnancies, identification of abnormalities in fetal growth or in amniotic fluid is central to antepartum care because the combination of surveillance and interventions could mitigate adverse outcomes.1,7,8,21

Our randomized trial differs from others on the topic26–30 vis-à-vis the enrollment criteria, the frequency of the ultrasound examinations in the intervention group, and the primary outcome being a composite of abnormalities of growth or amniotic fluid. Prior randomized trials on ultrasound examination after 24 weeks of gestation focused on either growth restriction26,28–30 or placental grading,27 whereas we focused on a composite of abnormal conditions and did not assess placental grade. With hypertensive disease of pregnancy, the fetus is primarily at risk for growth restriction and oligohydramnios, whereas in diabetes, the risks are primarily those of macrosomia and polyhydramnios.26,28–30 Among uncomplicated pregnancies, however, it is uncertain which aspect of abnormality in growth or amniotic fluid predominates. It is also noteworthy to mention that most of the prior randomized trials on the topic were done in the 1980s to 1990s26–28 or abroad26,27,29,30 and do not reflect contemporary practice in the United States.

The limitations of this randomized trial should be acknowledged. The likelihood of identifying individual component of the composite primary outcome of fetal growth abnormalities or oligohydramnios was similar in both groups, perhaps as a result of the sample size. Nonetheless, the trend was toward improved identification of abnormal growth with serial ultrasound examinations. Previous reports, however, have described the accuracy of identifying fetal growth restriction and LGA with ultrasound examinations.1,2,6,9,22,29,30 This single-center trial was not powered to detect differences in any obstetric or neonatal outcomes. Considering the infrequent rate of morbidity with uncomplicated pregnancies,10,12,13 a large multicenter randomized trial is required to demonstrate improvement, if any, in outcomes. All of the ultrasound examinations were done by registered diagnostic medical ultrasonography-certified ultrasonographers; hence, our findings may not be applicable to women who have third-trimester ultrasound examinations by clinicians during prenatal visits.31 The study was done at a tertiary, urban teaching center, where the population and clinical practice differ from other locations. We acknowledge that another limitation of this randomized trial is that the participants and clinicians were not blinded to group allocation. This shortcoming, however, permits us to ascertain the changes in clinical practices and outcomes if the clinical practice of routine third-trimester ultrasound examinations was implemented in uncomplicated pregnancies. Optimally, the chart abstractor should have been blinded to the group allocation, but the limited resources and pragmatic design precluded this option. Nonetheless, it should be noted that the determination of the primary and secondary composite outcomes was not determined by the chart abstractor. Lastly, we did not undertake a cost-effective analysis to determine whether the intervention justifies the cost.

The strengths of this randomized trial are notable. Unlike the prior pilot study,6 we calculated the sample size to ascertain whether serial ultrasound examinations do improve identification of abnormality of growth or amniotic fluid. The cohort of women we recruited was diverse. Our definitions of abnormality of fetal growth or amniotic fluid were consistent with the criteria promulgated by ACOG1,21 and reflect current clinical practice. The lost to follow-up was less than 1%. Being a randomized trial in which neither participants nor clinicians were blinded, our results provide reasonable estimates of the rate of the composite outcomes of fetal growth restriction, LGA, oligohydramnios, or polyhydramnios in uncomplicated pregnancies that are managed routinely or with serial ultrasound examinations in the third trimester.

Our trial should be a nidus for a larger multicenter trial with sufficient power to determine whether serial ultrasound examinations improve peripartum outcomes. Previously, investigators suggested that a trial of 6,000 low-risk pregnancies, randomized to routine care compared with serial ultrasound examination, has the power to detect a 36% difference, assuming the risk of neonatal morbidity is approximately 4% in the control arm.32 The sample size would be larger if a different outcome is used10 and if crossover from one group to another is accounted for. Such a large trial would permit better assessment of costs of serial scans (including interventions) in terms of charges to the patient and resource utilization. The larger trial may also demonstrate potential maternal benefits such as a decreased rate of cesarean delivery or greater satisfaction.33

In conclusion, among pregnancies without complications at 24 0/7 to 30 6/7 weeks of gestation, serial third-trimester ultrasound examinations were more likely to identify abnormalities of fetal growth or of amniotic fluid than measurements of fundal height. Before the clinical practice of serial ultrasound examinations is implemented in uncomplicated pregnancies, a larger randomized controlled trial is warranted.32

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